Comparative study of cartilaginous fish divulges insights into the early evolution of primary, secondary and mucosal lymphoid tissue architecture

Mitchell, Christian D.; Criscitiello, Michael F.

doi:10.1016/j.fsi.2020.11.006

Cited by 24 publications

(13 citation statements)

References 104 publications

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“…As gut tissues may be in contact with food and potential associated pathogens from the external environment, innate immunity and immune responses involved in digestion may help to protect the fish from food or environment related pathogens (97). Cartilaginous fishes have gut-associated lymphoid tissues in the spiral valve (98,99), consistent with the present observations of innate immune-related transcripts in the lake sturgeon spiral valve. Gene ontology terms related to toll-like receptor signaling pathways and cellular responses to interleukin were unique to the spiral valve in lake sturgeon, while terms related to innate immune function were also present in the muscular stomach, glandular stomach, and anterior intestine.…”

Section: Discussionsupporting

confidence: 92%

Tissue-specific transcriptomes reveal mechanisms of microbiome regulation in an ancient fish

Thorstensen

Weinrauch

Bugg

et al. 2022

Preprint

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The lake sturgeon (Acipenser fulvescens) is an ancient, octoploid fish faced with conservation challenges across its range in North America but a lack of genomic resources has hindered molecular research in the species. To support such research we aimed to provide a transcriptomic database from 13 tissues: brain, esophagus, gill, head kidney, heart, white muscle, liver, glandular stomach, muscular stomach, anterior intestine, pyloric cecum, spiral valve, and rectum. The transcriptomes for each tissue were sequenced and assembled individually from a mean of 98.3 million (38.9 million std. dev.) reads each. In addition, an overall transcriptome was assembled and annotated with all data used for each tissue-specific transcriptome. All assembled transcriptomes and their annotations were made publicly available as a scientific resource. The non-gut transcriptomes provide important resources for many research avenues, however, the gut represents a compartmentalized organ system with compartmentalized functions and the sequenced gut tissues were from each of these portions. Therefore, we focused our analysis on mRNA transcribed in different tissues of the gut and explored evidence of microbiome regulation. Gene set enrichment analyses were used to reveal the presence of photoperiod and circadian-related transcripts in the pyloric caecum, which may support periodicity in lake sturgeon digestion. Similar analyses were used to identify different types of innate immune regulation across the gut, while analyses of unique transcripts annotated to microbes revealed heterogeneous genera and genes among different gut tissues. The present results provide a scientific resource and information about the mechanisms of compartmentalized function across gut tissues in a phylogenetically ancient vertebrate.

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Section: Discussionsupporting

confidence: 92%

Tissue-specific transcriptomes reveal mechanisms of microbiome regulation in an ancient fish

Thorstensen

Weinrauch

Bugg

et al. 2022

Preprint

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“…This behavior was expected, as chemical induction of inflammation in zebrafish has previously been linked to the overexpression of PMN leukocytes, particularly the most abundant type, the neutrophils ( 71 ). Our results collectively conceive the peritoneum as an organ with lymphoid characteristics, which causes migration and stimulation of the immune cell, leading to powerful inflammatory reactions as previously suggested in mammals ( 72 ) and, more recently, in fish ( 73 ).…”

Section: Resultssupporting

confidence: 85%

Plasma proteome responses in zebrafish following λ-carrageenan-Induced inflammation are mediated by PMN leukocytes and correlate highly with their human counterparts

et al. 2022

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Regulation of inflammation is a critical process for maintaining physiological homeostasis. The λ-carrageenan (λ-CGN) is a mucopolysaccharide extracted from the cell wall of red algae (Chondrus crispus) capable of inducing acute intestinal inflammation, which is translated into the production of acute phase reactants secreted into the blood circulation. However, the associated mechanisms in vertebrates are not well understood. Here, we investigated the crucial factors behind the inflammatory milieu of λ-CGN-mediated inflammation administered at 0, 1.75, and 3.5% (v/w) by i.p. injection into the peritoneal cavity of adult zebrafish (ZF) (Danio rerio). We found that polymorphonuclear leukocytes (neutrophils) and lymphocytes infiltrating the ZF peritoneal cavity had short-term persistence. Nevertheless, they generate a strong pattern of inflammation that affects systemically and is enough to produce edema in the cavity. Consistent with these findings, cell infiltration, which causes notable tissue changes, resulted in the overexpression of several acute inflammatory markers at the protein level. Using reversed-phase high-performance liquid chromatography followed by a hybrid linear ion-trap mass spectrometry shotgun proteomic approach, we identified 2938 plasma proteins among the animals injected with PBS and 3.5% λ-CGN. First, the bioinformatic analysis revealed the composition of the plasma proteome. Interestingly, 72 commonly expressed proteins were recorded among the treated and control groups, but, surprisingly, 2830 novel proteins were differentially expressed exclusively in the λ-CGN-induced group. Furthermore, from the commonly expressed proteins, compared to the control group 62 proteins got a significant (p < 0.05) upregulation in the λ-CGN-treated group, while the remaining ten proteins were downregulated. Next, we obtained the major protein-protein interaction networks between hub protein clusters in the blood plasma of the λ-CGN induced group. Moreover, to understand the molecular underpinnings of these effects based on the unveiled protein sets, we performed a bioinformatic structural similarity analysis and generated overlapping 3D reconstructions between ZF and humans during acute inflammation. Biological pathway analysis pointed to the activation and abundance of diverse classical immune and acute phase reactants, several catalytic enzymes, and varied proteins supporting the immune response. Together, this information can be used for testing and finding novel pharmacological targets to treat human intestinal inflammatory diseases.

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“…Sharks and camelids diversify T cell receptors (TCR) by incorporating AID-mediated somatic mutations during thymic development, likely to salvage receptors that otherwise would fail selection (Antonacci et al 2011 ; Chen et al 2012 ; Ciccarese et al 2014 ; Ott et al 2018 , 2020 ). Finally, lamprey and hagfish utilize AID-like enzymes (CD1/CD2) to somatically rearrange variable lymphocyte receptor (VLR) loci to create diverse lymphocyte receptors (Mitchell and Criscitiello 2020 ; Pancer et al 2004 , 2005 ).…”

Section: Discussionmentioning

confidence: 99%

Evolution of immunogenetic components encoding ultralong CDR H3

et al. 2023

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The genomes of most vertebrates contain many V, D, and J gene segments within their Ig loci to construct highly variable CDR3 sequences through combinatorial diversity. This nucleotide variability translates into an antibody population containing extensive paratope diversity. Cattle have relatively few functional VDJ gene segments, requiring innovative approaches for generating diversity like the use of ultralong-encoding IGHV and IGHD gene segments that yield dramatically elongated CDR H3. Unique knob and stalk microdomains create protracted paratopes, where the antigen-binding knob sits atop a long stalk, allowing the antibody to bind both surface and recessed antigen epitopes. We examined genomes of twelve species of Bovidae to determine when ultralong-encoding IGHV and IGHD gene segments evolved. We located the 8-bp duplication encoding the unique TTVHQ motif in ultralong IGHV segments in six Bovid species (cattle, zebu, wild yak, domestic yak, American bison, and domestic gayal), but we did not find evidence of the duplication in species beyond the Bos and Bison genera. Additionally, we analyzed mRNA from bison spleen and identified a rich repertoire of expressed ultralong CDR H3 antibody mRNA, suggesting that bison use ultralong IGHV transcripts in their host defense. We found ultralong-encoding IGHD gene segments in all the same species except domestic yak, but again not beyond the Bos and Bison clade. Thus, the duplication event leading to this ultralong-encoding IGHV gene segment and the emergence of the ultralong-encoding IGHD gene segment appears to have evolved in a common ancestor of the Bos and Bison genera 5–10 million years ago. Supplementary Information The online version contains supplementary material available at 10.1007/s00251-023-01305-9.

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Comparative study of cartilaginous fish divulges insights into the early evolution of primary, secondary and mucosal lymphoid tissue architecture

Cited by 24 publications

References 104 publications

Tissue-specific transcriptomes reveal mechanisms of microbiome regulation in an ancient fish

Tissue-specific transcriptomes reveal mechanisms of microbiome regulation in an ancient fish

Plasma proteome responses in zebrafish following λ-carrageenan-Induced inflammation are mediated by PMN leukocytes and correlate highly with their human counterparts

Evolution of immunogenetic components encoding ultralong CDR H3

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